Skip to main content
Log in

Bt Proteins Have No Detrimental Effects on Larvae of the Green Lacewing, Chrysopa pallens (Rambur) (Neuroptera: Chrysopidae)

  • Ecology, Behavior and Bionomics
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

Biosafety of a genetically modified crop is required to be assessed prior to its commercialization. For this, a suitable artificial diet was developed and used to establish a dietary exposure test for assessing the toxicity of midgut-active Bt insecticidal proteins on Chrysopa pallens (Rambur). Subsequently, this dietary exposure test was used to evaluate the toxicity of the proteins Cry1Ab, Cry1Ac, Cry1Ah, Cry1Ca, Cry1F, Cry2Aa, Cry2Ab, and Vip3Aa on C. pallens larvae. Temporal stability, bioactivity, and the intake of the insecticidal proteins were confirmed by enzyme-linked immunosorbent assay and a sensitive-insect bioassay. The life history characteristics, such as survival, pupation, adult emergence, 7-day larval weight, larval developmental time, and emerged male and female fresh weights remained unaffected, when C. pallens were fed the pure artificial diet (negative control) and the artificial diets containing 200 μg/g of each purified protein: Cry1Ab, Cry1Ac, Cry1Ah, Cry1Ca, Cry1F, Cry2Aa, Cry2Ab, or Vip3Aa. On the contrary, all of the life history characteristics of C. pallens larvae were adversely affected when fed artificial diet containing boric acid (positive control). The results demonstrate that diets containing the tested concentrations of Cry1Ab, Cry1Ac, Cry1Ah, Cry1Ca, Cry1F, Cry2Aa, Cry2Ab, and Vip3Aa have null effects on C. pallens larvae. The outcome indicates that genetically modified crops expressing the tested Bt proteins are safe for the lacewing, C. pallens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adamczyk JJ, Gore J (2004) Laboratory and field performance of cotton containing Cry1Ac, Cry1F, and both Cry1Ac and Cry1F (Widestrike®) against beet armyworm and fall armyworm larvae (Lepidoptera: Noctuidae). Fla Entomol 87:427–432

    Article  CAS  Google Scholar 

  • Ali I, Zhang S, Cui JJ (2016) Bio-safety evaluation of Cry1Ac, Cry2Ab, Cry1Ca, Cry1F and Vip3Aa on Harmonia axyridis larvae. J Appl Entomol. doi:10.1111/jen.12309

    Google Scholar 

  • Alvarez-Alfageme F, Bigler F, Romeis J (2011) Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Res 20:467–479

    Article  CAS  PubMed  Google Scholar 

  • Buntin GD (2008) Corn expressing Cry1ab or Cry1f endotoxin for fall armyworm and corn earworm (Lepidoptera: Noctuidae) management in field corn for grain production. Fla Entomol 91:523–530

    Google Scholar 

  • Cohen AC, Smith LK (1998) A new concept in artificial diets for Chrysoperla rufilabris: the efficacy of solid diets. Biol Control 13:49–54

    Article  Google Scholar 

  • Conner AJ, Glare TR, Nap JP (2003) The release of genetically modified crops into the environment—part II. Overview of ecological risk assessment. Plant J 33:19–46

    Article  PubMed  Google Scholar 

  • Daane KM, Yokota GY, Zheng Y, Hagen KS (1996) Inundative release of common green lacewings (Neuroptera: Chrysopidae) to suppress Erythroneura variabilis and E-elegantula (Homoptera: Cicadellidae) in vineyards. Environ Entomol 25:1224–1234

    Article  Google Scholar 

  • Dutton A, Klein H, Romeis J, Bigler F (2002) Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol Entomol 27:441–447

    Article  Google Scholar 

  • Esteves Filho AB, Oliveira JV, Torres JB, Gondim MG Jr (2010) Biologia comparada e comportamento de Tetranychus urticae Koch (Acari: Tetranychidae) e Phytoseiulus macropilis (Banks)(Acari: Phytoseiidae) em algodoeiro bollgard TM e isolinha não-transgênica. Neotrop Entomol 39:338–344

    Article  PubMed  Google Scholar 

  • Gupta GP, Birah A, Rani S (2004) Development of artificial diet for mass rearing of American bollworm, Helicoverpa armigera. Indian J Agric Sci 74:548–551

    Google Scholar 

  • Hails RS (2002) Assessing the risks associated with new agricultural practices. Nature 418:685–688

    Article  CAS  PubMed  Google Scholar 

  • Hilbeck A, Baumgartner M, Fried PM, Bigler F (1998) Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae). Environ Entomol 27:480–487

    Article  Google Scholar 

  • James C, Teng P, Arujanan M, Aldemita RR, Flavell RB, Brookes G, Qaim M (2016) Invitational essays to celebrate the 20th anniversary of the commercialization of biotech crops (1996 to 2015): progress and promise

  • Koch MS, Ward JM, Levine SL, Baum JA, Vicini JL, Hammond BG (2015) The food and environmental safety of Bt crops. Front Plant Sci 6:283

    PubMed  PubMed Central  Google Scholar 

  • Kumar R, Tian J-C, Naranjo SE, Shelton AM (2014) Effects of Bt cotton on Thrips tabaci (Thysanoptera: Thripidae) and its predator, Orius insidiosus (Hemiptera: Anthocoridae). J Econ Entomol 107:927–932

    Article  PubMed  Google Scholar 

  • Lawo NC, Wackers FL, Romeis J (2010) Characterizing indirect prey-quality mediated effects of a Bt crop on predatory larvae of the green lacewing, Chrysoperla camea. J Insect Physiol 56:1702–1710

    Article  CAS  PubMed  Google Scholar 

  • Lawo NC, Wäckers FL, Romeis J (2009) Indian Bt cotton varieties do not affect the performance of cotton aphids. PLoS One 4:e4804

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee KS, Lee JH (2005) Rearing of Chrysopa pallens (Rambur) (Neuroptera: Chrysopidae) on artificial diet. Entomol Res 35:183–188

    Article  Google Scholar 

  • Li Y, Romeis J (2010) Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol Control 53:337–344

    Article  CAS  Google Scholar 

  • Li YH, Hu L, Romeis J, Wang YA, Han LZ, Chen XP, Peng YF (2014) Use of an artificial diet system to study the toxicity of gut-active insecticidal compounds on larvae of the green lacewing Chrysoperla sinica. Biol Control 69:45–51

    Article  CAS  Google Scholar 

  • Liu S, Wang S, Liu B, Zhou C, Zhang F (2011) The predation function response and predatory behavior observation of Chrysopa pallens larva to Bemisia tabaci. Sci Agric Sin 6:010

    Google Scholar 

  • Liu X, Chen M, Collins HL, Onstad DW, Roush RT, Zhang Q, Earle ED, Shelton AM (2014) Natural enemies delay insect resistance to Bt crops. PLoS One 9:e90366

    Article  PubMed  PubMed Central  Google Scholar 

  • Naranjo SE (2014) Effects of GM crops on non-target organisms. In: Plant biotechnology. Springer, Berlin Heidelberg New York, pp 129–142

    Google Scholar 

  • Nasreen A, Ashfaq M, Mustafa G, Khan RR (2007) Mortality rates of five commercial insecticides on Chrysoperla carnea (Stephens)(Chrysopidae: Neuroptera). Pak J Agric Sci 44:2

    Google Scholar 

  • Nasreen A, Cheema GM, Iqbal M (2005) Relative toxicity of different fungicides against larvae of green lacewing, Chrysoperla carnea (Chrysopidae: Neuroptera). S Pac Stud 26:7–13

    Google Scholar 

  • Porcar M, Garcia-Robles I, Dominguez-Escriba L, Latorre A (2010) Effects of Bacillus thuringiensis Cry1Ab and Cry3Aa endotoxins on predatory Coleoptera tested through artificial diet-incorporation bioassays. Bull Entomol Res 100:297–302

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Romero R, Desneux N, Chaufaux J, Kaiser L (2008) Bt-maize effects on biological parameters of the non-target aphid Sitobion avenae (Homoptera: Aphididae) and Cry1Ab toxin detection. Pestic Biochem Physiol 91:110–115

    Article  CAS  Google Scholar 

  • Rodrigo-Simon A, Ferre J (2006) A microscopic approach to determine the impact of Bacillus thuringiensis cry proteins on non-target organisms: lack of Cry1Ac binding to Chrysoperla carnea (Stephens) midgut epithelial cells. IOBC WPRS Bull 29:125

    Google Scholar 

  • Romeis J, Meissle M (2011) Non-target risk assessment of Bt crops—Cry protein uptake by aphids. J Appl Entomol 135:1–6

    Article  CAS  Google Scholar 

  • Romeis J, Meissle M, Naranjo SE, Li Y, Bigler F (2014) The end of a myth-Bt (Cry1Ab) maize does not harm green lacewings. Front Pl Sci 5:391

    Google Scholar 

  • Romeis J, Raybould A, Bigler F, Candolfi MP, Hellmich RL, Huesing JE, Shelton AM (2013) Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant genetically engineered crops. Chemosphere 90:901–909

    Article  CAS  PubMed  Google Scholar 

  • Sabry K, Ei-sayed A (2011) Biosafety of a biopesticide and some pesticides used on cotton crop against green lacewing, Chrysoperla carnea (Stehens) (Neuroptera: Chrysopidae). J Biopestic 4:214–218

    CAS  Google Scholar 

  • Sattar M, Fatima B, Ahmed N, Abro GH (2007) Development of larval artificial diet of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Pak J Zool 39:103–107

    CAS  Google Scholar 

  • Shrestha G, Enkegaard A (2013) The green lacewing, Chrysoperla carnea: Preference between lettuce aphids, Nasonovia ribisnigri, and western flower thrips, Frankliniella occidentalis. J Insect Sci 13

  • Stewart CN Jr, Richards HA, Halfhill MD (2000) Transgenic plants and biosafety: science, misconceptions and public perceptions. BioTechniques 29(832–836):838–843

    Google Scholar 

  • Szentkirályi F, McEwen P, New T, Whittington A (2001) Ecology and habitat relationships. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Toenniessen GH, O'Toole JC, DeVries J (2003) Advances in plant biotechnology and its adoption in developing countries. Curr Opin Plant Biol 6:191–198

    Article  PubMed  Google Scholar 

  • Torres JB, Ruberson JR, Adang MJ (2006) Expression of Bacillus thuringiensis Cry1Ac protein in cotton plants, acquisition by pests and predators: a tritrophic analysis. Agric For Entomol 8:191–202

    Article  Google Scholar 

  • Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS (2008) Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. Plos One 3

  • Xue J, Liang G, Crickmore N, Li H, He K, Song F, Feng X, Huang D, Zhang J (2008) Cloning and characterization of a novel Cry1A toxin from Bacillus thuringiensis with high toxicity to the Asian corn borer and other lepidopteran insects. FEMS Microbiol Lett 280:95–101

    Article  CAS  PubMed  Google Scholar 

  • Yang NW, Zang LS, Wang S, Guo JY, Xu HX, Zhang F, Wan FH (2014) Biological pest management by predators and parasitoids in the greenhouse vegetables in China. Biol Control 68:92–102

    Article  Google Scholar 

  • Zhao Q, Chen J, Liu F-X, Xiao W-F, Peng Y (2008) Predation of Chrysopa pallens on Myzus persicae and Aphis nerii. J Environ Entomol 3:005

    Google Scholar 

Download references

Acknowledgements

This study was funded by the Transgenic Major Projects Program of the Ministry of Science and Technology, China (2014ZX08011-002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I Ali.

Additional information

Edited by Jorge B Torres – UFRPE

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ali, I., Zhang, S., Muhammad, M.S. et al. Bt Proteins Have No Detrimental Effects on Larvae of the Green Lacewing, Chrysopa pallens (Rambur) (Neuroptera: Chrysopidae). Neotrop Entomol 47, 336–343 (2018). https://doi.org/10.1007/s13744-017-0526-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-017-0526-y

Keywords

Navigation